Accompanying the dramatic age-related decline in female fertility is a concomitant increase in the proportion of poor-quality oocytes that remain within the ovary. Based on the known proteomic changes that occur during oocyte ageing, and extrapolating from somatic cell literature, we hypothesised that a key contributor to the deterioration of oocyte quality is dysfunction of the essential protein degradation pathway known as autophagy. Thus, the aim of this study was to characterise autophagy in young and aged oocytes using a well-established mouse model of female reproductive ageing. Two primary autophagy pathway markers were assessed in this model; microtubule-associated protein 1 light chain 3B (LC3B), a constituent of the autophagosome membrane, and Beclin 1 (BECN1), an initiator of autophagosome formation. In addition, functional in vitro maturation studies were performed on pre-ovulatory germinal vesicle stage oocytes subjected to autophagy inhibition to assess oocyte maturation potential. This study revealed an increased number of large puncta (foci) containing LC3B and BECN1 in aged oocytes compared to young oocytes (n=3, p=0.046 and p=0.045 respectively). This was accompanied by a change in the localisation of LC3B and BECN1 puncta to favour the periphery of aged oocytes (n=3, p=0.029 and p=0.081 respectively). The use of the macroautophagy inhibitor, 3-methyladenine, led to a 27% reduction in the number of oocytes reaching the post-ovulatory metaphase II stage and extruding a polar body (n=3, p=0.044), indicative of meiotic failure. These findings shed light on the altered autophagy mechanisms occurring in aged oocytes and reveal an important role for autophagy in ensuring the competence of oocytes to mature to the post-ovulatory stage of development, a requisite for fertilization. This establishes the importance of autophagy in oocyte maturation and emphasises the need to further investigate the contribution of dysregulated autophagy pathways to age-related female infertility.